Becoming a shark: the hardships and mysteries of shark reproduction

Species living in the sea differ in many respects from those on land. Fishes not only developed special respiratory organs to extract oxygen from water, but also different ways of reproduction than mammals. Sharks even
have three different reproductive modes: viviparity, oviparity and ovoviparity. Viviparity is seen as a more advanced level of reproduction than ovi- and ovoviparity. It probably evolved in a more recent stage of evolution in certain species
for which which the benefits of increasing offspring survival exceeded the costs of reduced mobility and the greater metabolic demands of carrying offspring throughout development.Viviparous sharks give birth to living pups connected
to a placenta just like in mammals. The hammerhead, bull, lemon and oceanic sharks for example are viparous.The opposite of viviparous is oviparous which are sharks that lay eggs, like reptiles. An example is the Jackson shark
that lays eggs that have the shape of a corkscrew. In cat sharks the leathery transparent eggs have the shape of a small purse. The third way of reproduction is ovoviviparity or aplacental viviparity. Ovoviparity is found in many
big sharks, like the tiger, sand tiger and great white shark. Here embryos develop inside eggs that are retained within the mother's body until they are ready to hatch. It is similar to viviparous but differs in that there is no placental
connection and the unborn young are nourished by egg yolk (see picture left). The young may eat non fertilised eggs or even other embryos in the uterus if the yolk sac is depleted. The pups of the sand tiger shark have the reputation to
eat most of the embryos of its siblings, leaving only very few pups in a litter survive until birth.

New techniques have been developed in the last decades that allow to map migratory routes of sharks with more precision, and to identify
their genetic identity. But the reproductive biology of elasmobranches is a highly complex process that is still not fully understood by marine biologists. One reason being that the nature of their habitats makes it very difficult to observe mating
in the field.

Shark mating In the eyes of the human observer shark mating does not look like an affectionate and loving sexual event at all. During copulation, the male shark will bite down on the female’s
flank or fins to stabilize himself enough and then wrap his body around the female to successfully insert one of his claspers for insemination. Although the shark is not an universally beloved animal like the dolphin, its hard not to
feel sorry for the female shark when we observe the mating proces. But we must keep in mind that mating in animals serves only one purpose, which is reproduction. So copulation will only take place when the female is in estrus (with Pan, that
ischimpanzees and bonobos as rare exceptions). Moreover, the mating behavior of the 'ferocious' male shark is not so different from that of the 'loveable' male dolphin, that also has a reputation of herding and sexual coercion to seduce
a female.

More mates, more dads. Female sharks often copulate with different sharks (called polyandry). This may lead to multiple paternity (MP), implying that one litter of sharks contains baby sharks
that are sired by different fathers. MP has recently been established by marine biologists taking DNA samples from adult females and their litters. It is the same technique for DNA
profiling that has been used in humans for kinship analysis, paternity testing and in forensic biology. There is however a substantial variation between species, with some species being predominantly polyandrous with
a litter dominated by a several fathers, and other species genetically monandrous with litters dominated by single father. Also within a species -such as leopard sharks living in the same territory- some litters are dominated by one
dad, while others are shared by two or even more dads. Mating with multiple partners and MP are more likely to occur in situations when males outnumber the females. Males may then often unite in groups herding or mobbing to subdue
the female. Which may further increase the level of stress of the female shark. Still, female sharks are known to migrate each year over great distances to breeding sites where males congregate in greater numbers.

Costs and end benefits
of polyandry. The evolutionary role of polyandry is still a matter of debate among marine biologists. What benefits could there be for a female shark in enduring sexual intercourse with multiple partners, with the risk of more
physical injuries? A direct positive benefit has been hard to establish so far. But three explanations seem to be accepted most widely, in the following order.

1. Females engage in polyandry to avoid the physical costs
such as harassment and injuries associated with avoidance rather than acceptance, which is also called convenience polyandry. The only benefit for the female shark then would be to keep the physical damage of mating within
limits. Stronger and bigger females might cope better with mating stress than weaker species, thus diminishing the physical costs for themselves and enhancing the chance of fertilization of a succesful offspring.

2. Females mate promiscuously
because there is little opportunity to evaluate a male’s fitness prior to procreation. Mating with several males will therefore increase the likelihood of at least one of the males contributing to an increased offspring survival rate. And it might contribute
to greate genetic diversity.

3. Females that take multiple partners create an environment that promote sperm competition, which ultimately might lead either increased fertilization success or perhaps better genes of their offspring.
Fertilization may happen right after the shark mates in which case the order of copulation determines when eggs are fertilized. But many elasmobranches have developed the ability to store the males sperm in specialized glands for long periods
(a year or more) before using the sperm to fertilize their ova. Storing sperm also decreases the need for mating repeatedly to fertilize all ova during the breeding season. And it may facilitate post-copulatory influences on paternity by allowing either sperm
competition, i.e. the competition among the ejaculates of different males, and possibly also the differential storage and utilization of sperm of different mates.

Taken together, it seems that multiple paternity depends
a variety of factors such as the reproductive mode differences between sharks species, the occurrence of sperm storage in some shark species as well as the rate of male encounter, which in turn is influenced by factors such as population density, aggregative
behaviour and site fidelity.

What about the puppies? After fertilization the pregnant female sharks will often move to more protected in-shore locations such as bays or mangrove forests, that are suitable
as nursery zones to deliver their pups. They then leave the pups, which already have the instinct and capacity to hunt smaller species in their habitat. In the nurseries the vulnerable shark pups bide their time until they are big enough
to venture out of their shelter. They also provide a shelter for juvenile sharks ranging from several months to five years in age with a place to feed and grow. Baby and juvenile sharks thus lack parental care, and will not mix
with adult sharks at the risk of being eaten by the bigger sharks, which may even include their own mothers. A team of researchers recently tagged nine baby great white sharks right off the coast of Long Island, which gave rise
to the suspicion that there's a nursery of this powerful species just outside of New York City! Even not so far from the Trump building.

Growing up Little sharks grow rapidly. This is especially true for the juvenile
tiger shark that shows a growth rate of around 1 meter per year and reaches maturity at a relatively young age. The average female tiger shark reaches maturity by age 5 and males by age 4. With an average length at birth of 1 meter, the adult tiger sharks
maximum size is typically between 380 & 450 cm, with a few individuals reaching 550 cm.Their rapid growth may be a strategy for reducing juvenile predation risk. Other shark species in the family of Carcharhinidae seem to follow the same (albeit
slower) growth pattern.